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Oxygen availability and motor unit activity in

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Article in European Journal of Applied Physiology and Occupational Physiology · November 1992
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Eur J Appl Physiol (1992) 64:552-556
Oxygen availability and motor unit activity in humans
Toshio Moritanil, W. Michael Sherman 2, Masashi Shibata i, Tamaki Matsumoto I, and Minoru Shinohara 3
1 Laboratory of Applied Physiology, College of Liberal Arts and Sciences, Kyoto University, Sakyo-ku, Kyoto 606, Japan
2 School of Health, Physical Education and Recreation, Ohio State University, Columbus, OH 43210, USA
3 Department of Health and Physical Education, Kyoto College of Art, Kyoto 606, Japan
Accepted January 30, 1992
Summary. Six men were studied to determine the inter-
relationships among blood supply, motor unit (MU) ac-
tivity and lactate concentrations during intermittent
isometric contractions of the hand grip muscles. The
subjects performed repeated contractions at 20°7o of
maximal voluntary contraction (MVC) for 2 s followed
by 2-s rest for 4 min with either unhindered blood circu-
lation or arterial occlusion given between the 1st and
2nd min. The simultaneously recorded intramuscular
MU spikes and surface electromyogram (EMG) data in-
dicated that mean MU spike amplitude, firing frequency
and the parameters of surface EMG power spectra
(mean power frequency and root mean square ampli-
tude) remained constant during the experiment with un-
hindered circulation, providing no electrophysiological
signs of muscle fatigue. Significant increases in mean
MU spike amplitude and frequency were, however, evi-
dent during the contractions with arterial occlusion.
Similar patterns of significant changes in the surface
EMG spectra parameters and venous lactate concentra-
tion were also observed, while the integrated force-time
curves remained constant. These data would suggest
that the metabolic state of the active muscles may have
played an important role in the regulation of MU re-
cruitment and rate coding patterns during exercise.
Key words: Motor unit - Recruitment - Rate coding -
Metabolism - Electromyogram frequency power spec-
tra
Introduction
Since the size principle of Henneman et al. (1965) was
first proposed for results from cat motoneurons, strong
evidence has been presented that in muscle contraction
there is a specific sequence of recruitment in order of
increasing motoneuron and motor unit (MU) size (Miln-
er-Brown et al. 1973; Freund et al. 1975; Kukulka and
Offprint requests to: T. Moritani
European
Joumal of Applied
Physiology and Occupational Physiology
© Springer-Verlag1992
Clamann 1981; De Luca et al. 1982). It has been well
documented that MU recruitment and firing frequency
(rate coding) depend primarily upon the level of force
and the speed of contraction. When low-threshold MU
are recruited, this has resulted in a muscle contraction
characterized by low force-generating capabilities and
high fatigue resistance. With requirements for greater
force and/or faster contraction, high-threshold-fatigua-
ble MU have been recruited (Freund et al. 1975; Henne-
man and Mendell 1981). However, Kukulka and Cla-
mann (1981) and Moritani et al. (1986a) have demon-
strated in human adductor pollicis muscle that for a
muscle group with mainly type I fibres, rate coding
played a more prominent role in force modulation. For
a muscle group composed of both type I and II fibres,
MU recruitment seems to have been the major mecha-
nism for generating extra force above 40% to 50% of
maximal voluntary contraction (MVC; De Luca et al.
1982; Kukulka and Clamann 1981; Moritani et al.
1986a; Moritani and Muro 1987).
During cycling exercise, an increase in plasma lactate
concentration has been shown to be already apparent at
approximately 50%-70% of the rate of maximal oxygen
uptake (1202max) and well before the aerobic capacity is
fully utilized (Jorfeldt et al. 1978; Wasserman et al.
1985; Sahlin et al. 1987). During an incremental exercise
test on a cycle ergometer, however, Sjogaard (1978) has
shown that the peak force for a pedal thrust was less
than 20% MVC at exercise intensities eliciting l)'Ozm~x
at 60 rpm. Despite these relatively low force outputs and
moderate speeds of contraction during cycling, glycogen
content of types IIa and IIb fibres has been found to be
progressively decreased (first in type IIa and finally type
IIb fibres) during prolonged submaximal exercise (Vol-
lestad et al. 1984). Furthermore, Gollnick et al. (1974)
have also shown that in isometric contractions, slow
twitch units are the only ones to be depleted of glycogen
at force developments up to 15%-20% MVC. Above
this level, fast twitch units are also depleted of glycogen.
This would suggest that with this type of muscle con-
traction the availability of oxygen and the developed
force has influenced recruitment of fast-twitch units

since b l o o d flow has b e e n s h o w n to be u s u a l l y restricted
d u r i n g sustained c o n t r a c t i o n s o f a b o u t 20% M V C
( H u m p h r e y s a n d L i n d 1963). T h u s , these available data,
w o u l d suggest that n o t only the force a n d speed of con-
traction, b u t also the availability of oxygen m a y affect
the r e c r u i t m e n t of high threshold M U .
The p u r p o s e of the present study was, therefore, to
d e t e r m i n e the inter-relationships a m o n g oxygen availa-
bility, m o t o r u n i t activity a n d b l o o d lactate c o n c e n t r a -
tions d u r i n g i n t e r m i t t e n t isometric c o n t r a c t i o n s o f the
h a n d g r i p muscle.
Methods
Subjects and experimental protocols. Six male subjects volun-
teered for this study. They were fully informed about the nature
of the experiments including possible risks and gave their written
informed consent. The subject was in a prone position on a table.
The maximal voluntary grip strength was then measured three
times with a modified grip strength dynamometer previously de-
scribed (Moritani et al. 1984) and the highest value was recorded
as maximal voluntary grip strength (MVC). In the control situa-
tion (CON), the subject performed repeated intermittent isometric
contractions at 20% of MVC (2-s contraction followed by 2-s rest
period) for 4 rain. In the experimental situation (EXP), the subject
performed the identical repeated intermittent isometric contrac-
tions for 4 min but with the circulation occluded between the 1st
and 2nd min and given unhindered circulation during the last
2 rain (Fig. 1). The arterial occlusion was induced by a pressure
cuff around the upper arm which was inflated to 200 mmHg
(26.7 kPa) within 4 s by a cuff inflator. Care was taken to elimi-
nate movement of the upper body by tightly strapping down the
subject's chest and lower torso to the table. Venous blood samples
were obtained from a catheter inserted proximally into the bra-
chial vein. Samples were taken every 30 s during CON and at ev-
ery 15 s during EXP. Blood was analysed for lactate enzymatically
in duplicate and averaged. The two experimental conditions were
chosen at random interspersed by 30 min.
Force and electromyogram recordings. During the whole experi-
ment, the force signal was amplified through a DC amplifier
(Grass 7P122, Massachusetts, USA) and displayed on a digital os-
cilloscope (Kikusui 5020A, Tokyo, Japan) placed within view of
the subject for visual feedback. The level and duration of the tar-
get force were marked on the oscilloscope. The force and EMG
signals were visually and continuously monitored by the experi-
menter for any artefacts by means of a Tektronix 4-channel, dual
EXERCISE PROTOCOLS
REPERTED INTERMITTENT ISOMETRIC CONTRRCTIONS
EXPERIMENTRL CONDITIONS CHOSEN RT RRNDOM
C0 N free circulation
EXP
occlusion at 200mmHg
Fig. 1. Diagram of experimental conditions and exercise protocol.
MVC, Maximal voluntary contraction; CON, control; EXP, ex-
perimental conditions
553
time storage oscilloscope (Tektronix, Texas, USA). The force sig-
nal was digitized at a sampling rate of 100 Hz via an A-D convert-
er. The surface EMG and intramuscular spike signals were digi-
tized at sampling rates of 1 and 20 kHz, respectively, with 16-bit
fast A-D converters paced by precision pulse train cards and
stored on a floppy disk by the use of an HP 9836 desk-top com-
puter (Hewlett Packard, Colorado, USA). The digitized force data
were then processed off line for every 15 s for calculation of the
force-time integral by the computer.
Surface EMG and intramuscular spike analyses. Our EMG instru-
mentation and analysis procedures have been described elsewhere
in more detail (Moritani et al. 1985, 1986b). Briefly myo-electric
signals were recorded from bipolar surface electrodes (6-ram pick-
up diameter with 2-cm interelectrode distance) placed over the bel-
ly of the flexor carpi radialis-palmaris longus muscle. Intramuscu-
lar MU spikes were also recorded from high impedance bipolar
fine wire electrodes inserted approximately 1.5 cm under the skin.
After correcting for DC offset, the simultaneously digitized sur-
face EMG signals and intramuscular spikes were displayed on a
computer screen for pattern recognition by the experimenter and
then subjected to further data processing.
To quantify the surface EMG signal amplitude and frequency
components, analyses of the frequency power spectra were per-
formed. For this purpose, a series of 2048 ms EMG data, time-
locked to the onset of force production associated with contrac-
tion, were processed with the Hanning window function and 512
point fast Fourier transform (FFT) to obtain power spectra. Thus,
each EMG power spectrum corresponding to each contraction was
used to determine the mean power frequency (MPF) and the root
mean square (rms) value of the signal amplitude. Similarly, the
time-locked intramuscular MU spikes were isolated by a window
discriminant subroutine and the total number of spikes and mean
intramuscular MU spike amplitude were thus determined. These
data were averged for every 15 s for each subject during the 4-min
intermittent isometric contractions under CON and EXP, respec-
tively. The data were pooled for the purpose of allowing statistical
inferences.
Statistical analysis. The results were analysed using the Student's
t-test for paired data. A significance level of P_0.05 was chos-
en.
Results
Lactate concentrations and force changes
G r o u p data o n lactate c o n c e n t r a t i o n s a n d force-time in-
tegral changes are presented in Fig. 2. D u r i n g C O N , ve-
n o u s p l a s m a lactate c o n c e n t r a t i o n s showed a slight ini-
tial increase which was followed by a n almost c o n s t a n t
value of a p p r o x i m a t e l y 1 . 9 m m o l . 1 - 1 . D u r i n g E X P ,
however, the lactate c o n c e n t r a t i o n s showed large a n d
statistically significant increases of a p p r o x i m a t e l y
3 m m o l - 1 - 1 , shortly after the release o f the arterial oc-
clusion a n d r e m a i n e d significantly elevated d u r i n g the
rest o f E X P . I n contrast, n o significant changes in the
force-time integrals were observed t h r o u g h o u t the 4 - m i n
i n t e r m i t t e n t isometric c o n t r a c t i o n s either d u r i n g C O N
or d u r i n g E X P (Fig. 2).
Changes in M U activities
A typical set of changes in the i n t r a m u s c u l a r M U spike
recordings is s h o w n in Fig. 3. O n l y 1-s samples o f M U
 554

CONTROL EXPERIMENTRL INTRAMUSCULAR

CONTROL EXPERIMENTBL
4
W W
~IQ 200
n- IT 3
150
U 2
IT"
_J _.1 o_] 100
1

B
~ so
B B 2 3 4
I 2 3 4 1
0
0 1 0 3 4 0 I ~ 3 4

5@ 50
250
40
z ~ 300 ~ 200
Z
W150
n.,
0
L
20 ,9 26 10o L~100
10 IB b_ 50 50

l 2 3 4rain 00 l 2 3 4min 00 1 2 3 4rnin 00 1 2 3 4min

TIME TIME TIME TIME

Fig. 2. Changes in force-time integrals and blood lactate concen- Fig. 4. Group data (mean and SEM, n = 6) showing the changes in
trations (mean and SEM, n = 6) during experiments with unhin- motor unit spike amplitudes and firing frequencies observed dur-
dered circulation (control) and arterial occlusion given between 1st ing unhindered circulation (control) and arterial occlusion (experi-
and 2nd rain (experimental) mental) trials

REM: OCCLUSION S U B :0 0 2
lease), the large MU spikes had disappeared and only
800 15s the low-amplitude MU spikes similar to those observed
488 at the beginning of the experiment without occlusion
0 seemed to be involved. During CON, on the other hand,
BBO [ 30s no such spontaneous changes in MU amplitude and
4BE] spike frequency were observed, but the analysis showed
almost constant MU activities with low-amplitude spikes
880 I 45s throughout the entire 4 min of intermittent isometric
480 exercise (Fig. 4). These finding were consistent and in-
6 ,gh,h,,*~*,L,.,d, = • variant features in all the subjects tested.
B00 60s Group data on mean MU spike amplitude and firing
400 frequency (number of MU spikes per second) are shown
B in Fig. 4. Nearly constant MU amplitude and firing fre-
s
I I si s s
•
i5 i
t 0 .5 1 .5 10 . 1 quency were maintained throughout the entire period of
TIME TIME TIME TIME exercise during CON. There were, as expected, no sig-
nificant differences in the MU spike amplitude and fre-
Fig. 3. A typical set of changes in the intramuscular spikes ob- quency between CON and EXP prior to the arterial oc-
served during experimental conditions (unhindered circulation clusion. However, significant increases in both MU
plus occlusion between 1st and 2nd min). In this figure only 1-s spike amplitude and firing frequency were observed not
samples of motor unit spikes obtained at every 15-s interval (raw only during the period of contractions with the occlu-
data) are given for clarity. Thus, in this figure each column repre-
sents 1 min of repeated intermittent isometric contraction sion, but also during the period of recovery up to 1 min
from the release of the occlusion (Fig. 4). During the 3rd
and 4th min into recovery, the mean MU spike ampli-
tude and frequency were still greater after occlusion
spikes obtained at every 15-s interval are presented for than during CON but these differences were not statisti-
clarity. During EXP, a consistent pattern of MU activity cally significant.
with similar low-amplitude spikes could be observed pri-
or to the arterial occlusion (Fig. 3, left panel and first
column top to bottom). There were, however, large and Surface EMG changes
progressive increases in both MU spike amplitude and
firing frequency during the period of arterial occlusion Figure 5 gives group data on the results of the analyses
(Fig. 3, second column top to bottom), suggesting new of the surface EMG power spectra during CON and
MU recruitment and increased MU discharge rate of re- EXP. The rms value of E M G amplitude and MPF
latively high-threshold units. It is noteworthy that the showed no systematic changes and stayed almost con-
large MU spike amplitudes observed during the occlu- stant at the end of the 2nd min until the end of the ex-
sion were still seen even 30 s after the complete release periment during CON. During EXP the relatively con-
of occlusion (e.g. Fig, 3, third column top three rows). stant rms values observed at the beginning of the experi-
By the end of the 3rd min (1 min after occlusion re- ment, however, showed progressive and significant in-

SURFACE EMG
CONTROL
150 [ 158[
1281-
98
5-
w 68 r¢ 6
3 38
0 t 2 3 4 88
~-~ 98 Ix.
60
n
'F"
30
88 [ 2 3 4 rain B l
TIME
Fig. 5. Group data (mean and SEM, n = 6) showingthe changes in
surface electromyogram (EMG) amplitude (root mean square,
rms) and mean power frequency(MPF) during unhindered circu-
lation (control) and arterial occlusion(experimental)trials
creases during the last 30 s of occlusion and reached
quite high values (approximately twofold increase) for
the next 60 s. These rms changes were followed by a pro-
gressive decline but the differences in the rms values be-
tween CON and EXP were still significant even at the
end of the 4-min period (Fig. 5, top right). The MPF
data also indicated similar results in that the relatively
stable MPF values observed during CON and prior to
the occlusion during EXP decreased significantly during
the last 30s of occlusion and remained depressed
throughout the rest of the experiment.
Discussion
In the present study, the constancy of both intramuscu-
lar MU spikes and surface EMG activity during isomet-
ric contraction indicated no electrophysiological signs of
muscle fatigue when the circulation was unhindered.
However, significant changes in these parameters were
evident during contractions with arterial occlusion.
Since the availability of oxygen and blood borne sub-
strates, e.g. glucose and free fatty acids, were severely
reduced during occlusion, a progressive recruitment of
additional MU might have taken place to compensate
for the deficit in force development (Bigland-Ritchie et
al. 1986; Moritani et al. 1986b). This may have occurred
if MU had become depleted of glycogen (Gollnick et al.
1974; Vollestad et al. 1984) or affected by some degree
of intramuscular acidification (Wilkie 1986; Metzger
and Moss 1987). This in turn would have interfered with
the excitation-contraction coupling with a subsequent
decrease in the force developed.
During a wide range of submaximal contractions not
all of the available MU pool is recruited. We have de-
monstrated that there was a progressive decrease in
MPF of the surface EMG signal during sustained con-
tractions at 50o7o of MVC but this decline was accompa-
555
nied by a significant increase in the rms value of the
EXPERIMENTRL EMG amplitude and a progressive MU recruitment as
evidenced by an increased number of MU with relatively
,
large intramuscular spike amplitudes (Moritani et al.
1986b). These results and the present findings of signifi-
8 ~
cant increases in MU firing rate and MU spike ampli-
tude associated with arterial occlusion thus suggest that
I 2 3 4 not only the force and speed of contraction but also the
availability of oxygen may have affected the recruitment
of high threshold MU. In good agreement with this hy-
pothesis, the 31p nuclear magnetic resonance experi-
ments (Bylund-Fellenius et al. 1981) have demonstrated
that the rate of recovery in phosphocreatine:inorganic
phosphate during the contraction was dependent on
oxygen delivery. These results and recent evidence (Id-
~ 3 4 min str6m et al. 1985; Katz and Sahlin 1987) would suggest a
TIME causal relationship between oxygen supply and energy
state in the contracting as well as in recovering skeletal
muscles. In consideration of this evidence, it might be
suggested that oxygen availability may have played an
important role in regulating MU recruitment and firing
frequency as there has been shown to exist a close link
between the state of energy supply and the types of mus-
cle fibres being recruited (IdstrOm et al. 1985; Bigland-
Ritchie et al. 1986; Moritani et al. 1985, 1986b).
At present, the specific messenger to which the motor
control system respond with varying patterns of MU re-
cruitment and firing frequency has not yet been clearly
established. There is some evidence that the order of
MU recruitment might be modified by changes in the
proprioceptive afferent activity (Grimby and Hannerz
1976; Garnett and Stephens 1981; Kitsch and Rymer
1987). The observed large and progressive increases in
both MU spike amplitude and firing frequency during
the period of arterial occlusion would suggest new MU
recruitment and an increased MU discharge rate of rela-
tively high-threshold units. This might thus have been
the result of such changes in the proprioceptive afferent
inputs of the affected muscle fibres to the motoneurons
as a consequence of severely reduced oxygen availability
and/or a strong pressure applied during the arterial oc-
clusion. However, the large MU spike amplitudes seen
during the occlusion were still seen, even after the com-
plete release of occlusion, for more than 30 s. Results
from a recent study (Rotto and Kaufman 1988) have
also shown that very large concentrations of sodium lac-
tate (much larger than the lactate changes we observed)
were required to stimulate group III and IV muscle af-
ferent nerves. Therefore, any effects of increased pres-
sure or metabolic by-products on the group III or IV af-
ferent nerve fibres that might modify MU recruitment
patterns could not have been major mechanisms for the
increased MU recruitment and firing frequency of rela-
tively high-threshold units.
Other and possibly more likely explanations might be
that the stretch receptors in muscle spindles and Golgi
tendon organs have signalled the need for adding more
MU (Enoka and Stuart 1985; Nelson and Hutton 1985;
Hutton and Nelson 1986; Kirsch and Rymer 1987) as a
result of a decrease in the contractility of some MU af-
fected by the reduced oxygen supply and/or depletion of
556
i n t r a m u s c u l a r glycogen stores ( G o l l n b i c k et al. 1974;
B y l u n d - F e l l e n i u s et al. 1981; V o l l e s t a d et al. 1984; Id-
strOm et al. 1985). O r there m a y have been s o m e in-
fluences o n the m o t o n e u r o n p o o l activity f r o m the sen-
s o r y a f f e r e n t nerve fibres o r i g i n a t i n g in the " m e t a b o r e -
c e p t o r s " ( M a h l e r 1979; S j o g a a r d 1990).
T h e n o n s i g n i f i c a n t increase o f venous b l o o d lactate
c o n c e n t r a t i o n d u r i n g the p e r i o d o f arterial occlusion is
very difficult to explain, p a r t i c u l a r l y in the absence o f
muscle lactate d a t a . It can o n l y b e s p e c u l a t e d t h a t the
venous b l o o d s a m p l e s o b t a i n e d d u r i n g arterial occlusion
m i g h t n o t have r e p r e s e n t e d the t i m e course o f changes
o f muscle lactate c o n c e n t r a t i o n . T h e significant in-
creases in b l o o d lactate c o n c e n t r a t i o n a f t e r the release
o f occlusion c o u l d t h e n be e x p l a i n e d as a result o f m u s -
cle lactate being w a s h e d o u t a f t e r the r e s t o r a t i o n o f
b l o o d flow.
I n s u m m a r y , o u r d a t a i n d i c a t e d a l t e r a t i o n o f M U fir-
ing a n d r e c r u i t m e n t p a t t e r n s d u r i n g c o n t r a c t i o n s with is-
c h a e m i a . It is suggested t h a t the m e t a b o l i c state o f the
active muscles m a y have p l a y e d an i m p o r t a n t role in the
r e g u l a t i o n o f M U r e c r u i t m e n t a n d rate c o d i n g p a t t e r n s
d u r i n g exercise.
Acknowledgements. This study was supported by the Japanese
Ministry of Education grant no. 60580099 and the Texas Engi-
neering Experiment Station grant no. 9058E.
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